Telomere fusion to chromosome breaks reduces oncogenic translocations and tumour formation

Nat Cell Biol. 2005 Jul;7(7):706-11. doi: 10.1038/ncb1276. Epub 2005 Jun 19.

Abstract

Telomeres protect chromosome ends from fusion, degradation and recombination. Loss of telomere function has opposite effects on tumorigenesis: apoptosis, which inhibits tumour growth, and genomic instability, which accelerates tumour formation. Here we describe a new mechanism by which short telomeres inhibit tumorigenesis through interference with oncogenic translocations. In mice that are null for both ataxia-telangiectasia-mutated (Atm) and telomerase RNA (mTR), the first generation (G1) Atm-/- mTR-/- mice have a lower rate of tumour formation than Atm-/- mTR+/+ mice. These Atm-/- mTR-/- G1 tumours show no increase in either apoptosis or overall genomic instability. Strikingly, the tumours show a high fraction of translocations containing telomere signals at the translocation junctions. Translocations of the T-cell receptors on chromosome 14, which initiate tumorigenesis, were interrupted by fusion with telomeres. Telomere repeats were also detected at the translocation junctions in pre-malignant thymocytes. We propose that telomere fusion to DNA double-strand breaks competes with the generation of oncogenic translocations and thus reduces tumour formation.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Age Factors
  • Animals
  • Apoptosis / genetics
  • Ataxia Telangiectasia Mutated Proteins
  • B-Lymphocytes / chemistry
  • B-Lymphocytes / metabolism
  • Body Weight / genetics
  • Cell Cycle Proteins / genetics
  • Cell Proliferation
  • Chromosome Breakage / genetics*
  • Crosses, Genetic
  • DNA-Binding Proteins / genetics
  • Female
  • Gene Rearrangement, T-Lymphocyte / genetics
  • Genes, T-Cell Receptor / genetics
  • Genomic Instability / genetics
  • Genotype
  • In Situ Hybridization, Fluorescence
  • Lymphoma, T-Cell / genetics
  • Lymphoma, T-Cell / pathology
  • Male
  • Mice
  • Mice, Knockout
  • Mice, SCID
  • Models, Genetic
  • Neoplasm Transplantation
  • Neoplasms, Experimental / genetics*
  • Neoplasms, Experimental / pathology
  • Protein Serine-Threonine Kinases / genetics
  • Spectral Karyotyping
  • Survival Analysis
  • Telomerase / genetics
  • Telomere / genetics
  • Telomere / metabolism*
  • Translocation, Genetic / genetics*
  • Tumor Suppressor Proteins / genetics

Substances

  • Cell Cycle Proteins
  • DNA-Binding Proteins
  • Tumor Suppressor Proteins
  • Ataxia Telangiectasia Mutated Proteins
  • Atm protein, mouse
  • Protein Serine-Threonine Kinases
  • Telomerase